Hippocampal-dependent navigation without outcome-sensitive control

Goal-directed decisions depend on predictions of future outcomes and are thus sensitive to revaluation of expected outcomes, whereas habitual decisions depend on cached action values or stimulus-response associations and are insensitive to outcome revaluation. Hippocampal neurons encode future states (potentially supporting prediction of future outcomes during goal-directed choice) as well as present states (potentially supporting retrieval of state-dependent action values during habitual choice). Prior studies suggest a role for the hippocampus in goal-directed, outcome-sensitive decision making, but few studies have examined its role in outcome-insensitive action selection. Here, we tested this using a two-outcome spatial navigation task in which identical turning actions (left or right) led either to preferred milk or non-preferred water outcomes, depending on the spatial location at which the choice was made. Rats (20 males, 22 females) were trained under conditions that either required hippocampal-dependent discrimination between choice points or allowed hippocampal-independent navigation using visual beacons. Rats then underwent 24 h water restriction during which separate cohorts underwent Contingency Updating (CU), in which rats re-experienced the maze action-outcome contingencies while thirsty, or Incentive Learning (IL), in which rats received only a two-bottle preference test while thirsty without re-experiencing maze contingencies. Both cohorts were later tested under thirst on an unbaited maze. CU rats shifted their choices toward water-associated responses, whereas IL rats perseverated on milk-associated responses, even when navigation depended on the hippocampus. These results provide novel evidence that hippocampal-dependent navigational decisions can show insensitivity to outcome revaluation, a widely used behavioral criterion for habitual control.Significance Statement We show here that the dorsal hippocampus can support navigational decisions that are insensitive to outcome revaluation during a spatial task in which identical actions lead to different outcomes depending on location. Even when the hippocampus was required for accurate navigation to reach a preferred outcome, rats extensively trained on this task failed to adjust their choices after revaluation altered their outcome preferences. To our knowledge, these findings provide the first direct evidence that hippocampal-dependent navigation can satisfy a widely used behavioral criterion for habitual control.